Skip to main content
Log in

Vertical canopy gradients in δ13C correspond with leaf nitrogen content in a mixed-species conifer forest

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Stable carbon isotope composition varies markedly between sun and shade leaves, with sun leaves being invariably more enriched (i.e., they contain more13C). Several hypotheses have emerged to explain this pattern, but controversy remains as to which mechanism is most general. We measured vertical gradients in stable carbon isotope composition (δ13C) in more than 200 trees of nine conifer species growing in mixed-species forests in the Northern Rocky Mountains, USA. For all species except western larch, δ13C decreased from top to bottom of the canopy. We found that δ13C was strongly correlated with nitrogen per unit leaf area (N area), which is a measure of photosynthetic capacity. Usually weaker correlations were found between δ13C and leaf mass per area, nitrogen per unit leaf mass, height from the ground, or depth in the canopy, and these correlations were more variable between trees than for N area. Gradients of δ13C (per meter canopy depth) were steeper in small trees than in tall trees, indicating that a recent explanation of δ13C gradients in terms of drought stress of upper canopy leaves is unlikely to apply in our study area. The strong relationship between N area and δ13C here reported is consistent with the general finding that leaves or species with higher photosynthetic capacity tend to maintain lower CO2 concentrations inside leaves. We conclude that photosynthetic capacity is a strong determinant of δ13C in vertical canopy profiles, and must be accounted for when interpreting δ13C values in conifer forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Beadle CL, Neilson RE, Talbot H, Jarvis PG (1985) Stomatal conductance and photosynthesis in a mature Scots pine forest I. Diurnal, seasonal and spatial variation in shoots. J App Ecol 22:557–571

    Article  Google Scholar 

  • Berry SC, Varney GT, Flanagan LB (1997) Leaf δ13C in Pinus resinosa trees and understorey plants: variation associated with light and CO2 gradients. Oecologia 109:499–506

    Article  Google Scholar 

  • Bonal D, Barigah TS, Granier A, Guehl JM (2000) Late-stage canopy tree species with extremely low δ13C and high stomatal sensitivity to seasonal soil drought in the tropical rainforest of French Guiana. Plant Cell Environ 23:445–459

    Article  Google Scholar 

  • Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance. Oecologia 120:183–192

    Article  Google Scholar 

  • Bowling DR, McDowell NG, Bond BJ, Law BE, Ehleringer JR (2002) 13C content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124

    Article  Google Scholar 

  • Broadmeadow MSJ, Griffiths H (1993) Carbon isotope discrimination and the coupling of CO2 fluxes within forest canopies. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant–water relations. Academic, New York, pp 109–129

    Google Scholar 

  • Brooks JR, Flanagan LB, Varney GT, Ehleringer JR (1997) Vertical gradients in photosynthetic gas exchange characteristics and refixation of respired CO2 within boreal forest canopies. Tree Physiol 17:1–12

    PubMed  Google Scholar 

  • Buchmann N, Brooks JR, Ehleringer JR (2002) Predicting daytime carbon isotope ratios of atmospheric CO2 within forest canopies. Funct Ecol 16:49–57

    Article  Google Scholar 

  • Cernusak LA, Marshall JD (2001) Responses of foliar δ13C, gas exchange and leaf morphology to reduced hydraulic conductivity in Pinus monticola branches. Tree Physiol 21:1215–1222

    PubMed  CAS  Google Scholar 

  • Cochard H, Lemoine D, Dreyer E (1999) The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L. Plant Cell Environ 22:101–108

    Article  Google Scholar 

  • Cooper SV, Neiman KE, Roberts DW (1991) Forest habitat types of Northern Idaho: a second approximation. USDA For Serv Gen Tech Rep INT-236

  • Cordell S, Goldstein G, Meinzer FC, Handley LL (1999) Allocation of nitrogen and carbon in leaves of Meterosideros polymorpha regulates carboxylation capacity and δ13C along an altitudinal gradient. Funct Ecol 13:811–818

    Article  Google Scholar 

  • Dang Q, Margolis HA, Coyea MR, Sy M, Collatz GJ (1997) Regulation of branch-level gas exchange of boreal trees: roles of shoot water potential and vapour pressure deficit. Tree Physiol 17:521–535

    PubMed  CAS  Google Scholar 

  • Duursma RA, Marshall JD, Robinson AP (2003) Leaf area index inferred from solar beam transmission in mixed conifer forests on complex terrain. Agric For Meteorol 118:221–236

    Article  Google Scholar 

  • Duursma RA, Marshall JD, Nippert JB, Chambers CC, Robinson AP (2005) Estimating leaf-level parameters for ecosystem process models: a study in mixed conifer canopies on complex terrain. Tree Physiol 25:1347–1359

    PubMed  Google Scholar 

  • Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Physiol 13:281–292

    CAS  Google Scholar 

  • Evans JR, Loreto F (2000) Acquisition and diffusion of CO2 in higher plant leaves. In: Leegood RC, Sharkey TD, von Caemmerer (eds) Photosynthesis: physiology and metabolism. Kluwer, Dordrecht, pp 321–351

    Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

    CAS  Google Scholar 

  • Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    CAS  Google Scholar 

  • Farquhar GD, Wong SC (1984) An empirical model of stomatal conductance. Aust J Plant Physiol 11:191–210

    CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol 40:503–537

    Article  CAS  Google Scholar 

  • Fessenden JE, Ehleringer JR (2003) Temporal variation in δ13C of ecosystem respiration in the Pacific Northwest: links to moisture stress. Oecologia 136:129–136

    Article  PubMed  Google Scholar 

  • Finklin AI (1983) Climate of Priest River Experimental Forest, northern Idaho. USDA For Serv Gen Tech Rep. INT-159

  • Francey RJ, Gifford RM, Sharkey TD, Weir B (1985) Physiological influences on carbon isotope discrimination in huon pine (Lagorostrobos franklinii). Oecologia 66:211–218

    Google Scholar 

  • Gillon JS, Borland AM, Harwood KG, Roberts A, Broadmeadow MSJ, Griffiths H (1998) Carbon isotope discrimination in terrestrial plants: carboxylations and decarboxylations. In: Griffiths H (ed) Stable isotopes. BIOS, Oxford

    Google Scholar 

  • Guehl JM, Aussenac G, Bouachrine J, Zimmermann R, Pennes JM, Ferhi A, Grieu P (1991) Sensitivity of leaf gas exchange to atmospheric drought, soil drought, and water-use efficiency in some Mediterranean Abies species. Can J For Res 21:1507–1515

    Article  Google Scholar 

  • Hanba YT, Mori S, Lei TT, Koike T, Wada E (1997) Variations in leaf δ13C along a vertical profile of irradiance in a temperate Japanese forest. Oecologia 110:253–261

    Article  Google Scholar 

  • Hanba YT, Kogami H, Terashima I (2003) The effect of internal CO2 conductance on leaf carbon isotope ratio. Isot Environ Health Stud 39:5–13

    Article  CAS  Google Scholar 

  • Harlow BA, Duursma RA, Marshall JD (2005) Leaf longevity of western red cedar (Thuja plicata) increases with depth in the canopy. Tree Physiol 25:635–640

    Google Scholar 

  • Hubbard RM, Bond BJ, Ryan MG (1999) Evidence that hydraulic conductance limits photosynthesis in old Pinus ponderosa trees. Tree Physiol 19:165–172

    PubMed  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123:32–40

    Article  Google Scholar 

  • Jarvis PG, James GB, Landsberg JJ (1976) Coniferous forest. In: Monteith JL (ed) Vegetation and the atmosphere, vol II. Academic, London, pp 171–240

    Google Scholar 

  • Jones HG (1992) Plants and microclimate, 2nd edn. Cambridge University Press, Cambridge, 428 p

    Google Scholar 

  • Katul GG, Ellsworth DS, Lai CT (2000) Modelling assimilation and intercellular CO2 from measured conductance: a synthesis of approaches. Plant Cell Environ 23:1313–1328

    Article  Google Scholar 

  • Koch GW, Sillett SC, Jennings GM, Davis SD (2004) Limits to tree height. Nature 428:851–854

    Article  PubMed  CAS  Google Scholar 

  • Kogami H, Hanba YT, Kibe T, Terashima I, Masuzawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant Cell Environ 24:529–538

    Article  CAS  Google Scholar 

  • Körner Ch, Scheel JA, Bauer H (1979) Maximum leaf diffusive conductance in vascular plants. Photosynthetica 13:45–82

    Google Scholar 

  • Kvålseth TO (1985) A cautionary note about R 2. Am Stat 39:279–285

    Article  Google Scholar 

  • Lamont BB, Groom PK, Cowling RM (2002) High leaf mass per area of related species assemblages may reflect low rainfall and carbon isotope discrimination rather than low phosphorus and nitrogen concentration. Funct Ecol 16:403–412

    Article  Google Scholar 

  • Lemoine D, Cochard H, Granier A (2002) Within crown variation in hydraulic architecture in beech (Fagus sylvatica L.): evidence for a stomatal control of xylem embolism. Ann For Sci 59:19–27

    Article  Google Scholar 

  • Le Roux X, Bariac T, Sinoquet H, Genty B, Piel C, Mariotti A, Girardin C, Richard P (2001) Spatial distribution of leaf water-use efficiency and carbon isotope discrimination within an isolated tree crown. Plant Cell Environ 24:1021–1032

    Article  Google Scholar 

  • Leuning R (1995) A critical appraisal of a combined stomatal-photosynthesis model for C3 plants. Plant Cell Environ 18:339–355

    Article  CAS  Google Scholar 

  • Li C, Liu S, Berninger F (2004) Picea seedlings show apparent acclimation to drought with increasing altitude in the eastern Himalaya. Trees 18:277–283

    Google Scholar 

  • Livingston NJ, Whitehead D, Kelliher FM, Wang YP, Grace JC, Walcroft AS, Byers JN, McSeveny TM, Millard P (1998) Nitrogen allocation and carbon isotope fractionation in relation to intercepted radiation and position in a young Pinus radiate D. Don. Tree Plant Cell Environ 21:795–803

    Article  CAS  Google Scholar 

  • Loustau D, Moussa FEH (1989) Variability of stomatal conductance in the crown of a maritime pine (Pinus pinaster Ait.). Ann Sci For 46S:426–428

    Article  Google Scholar 

  • MacFarlane C, Adams MA, White DA (2004) Productivity, carbon isotope discrimination and leaf traits of trees of Eucalyptus globulus Labill. in relation to water availability. Plant Cell Environ 27:1515–1524

    Article  Google Scholar 

  • Marshall JD, Zhang J (1994) Carbon isotope discrimination and water use efficiency of native plants of the north-central Rockies. Ecology 75:1887–1895

    Article  Google Scholar 

  • Marshall JD, Monserud RA (2003) Foliage height influences specific leaf area of three conifer species. Can J For Res 33:164–170

    Article  Google Scholar 

  • Martin TA, Hinckley TM, Meinzer FC, Sprugel DG (1999) Boundary layer conductance, leaf temperature and transpiration of Abies amabilis branches. Tree Physiol 19:435–443

    PubMed  Google Scholar 

  • Mencuccini M, Grace J (1996) Developmental patterns of above-ground hydraulic conductance in a Scots pine (Pinus sylvestris L.) age sequence. Plant Cell Environ 19:939-948

    Article  Google Scholar 

  • Monclus R, Dreyer E, Delmotte FM, Villar M, Delay D, Boudouresque E, Petit J, Marron N, Bréchet C, Brignolas F (2005) Productivity, leaf traits and carbon isotope discrimination in 29 Populus deltoides x P. nigra clones. New Phytol 167:53–62

    Article  PubMed  Google Scholar 

  • Meinzer FC (1982) The effect of light on stomatal control of gas exchange in Douglas fir (Pseudotsuga menziesii) saplings. Oecologia 54:270–274

    Article  Google Scholar 

  • Monserud RA, Marshall JD (1999) Allometric crown relations in three northern Idaho conifer species. Can J For Res 29:521–535

    Article  Google Scholar 

  • Niinemets Ü (1997a) Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies. Trees 11:144–154

    Article  Google Scholar 

  • Niinemets Ü (1997b) Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species. Funct Ecol 11:518–531

    Article  Google Scholar 

  • Niinemets Ü, Kull O, Tenhunen JD (1998) An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiol 18:681–696

    PubMed  Google Scholar 

  • Niinemets Ü, Kull O, Tenhunen JD (1999) Variability in leaf morphology and chemical composition as a function of canopy light environment in coexisting deciduous trees. Int J Plant Sci 160:837–848

    Article  PubMed  Google Scholar 

  • Niinemets Ü, Sonninen E, Tobias M (2004a) Canopy gradients in leaf intercellular CO2 mole fractions revisited: interactions between leaf irradiance and water stress need consideration. Plant Cell Environ 27:569–583

    Article  Google Scholar 

  • Palmroth S, Hari P (2001) Evaluation of the importance of acclimation of needle structure, photosynthesis, and respiration to available photosynthetically active radiation in a Scots pine canopy. Can J For Res 31:1235–1243

    Article  Google Scholar 

  • Parker GG, Davis MM, Chapotin SM (2002) Canopy light transmittance in Douglas-fir-western hemlock stands. Tree Physiol 22:147–157

    PubMed  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, Berlin Heidelberg New York, 528 p

    Google Scholar 

  • Pocewicz AL, Gessler P, Robinson AP (2004) The relationship between effective plant area index and Landsat spectral response across elevation, solar insolation, and spatial scales in a northern Idaho forest. Can J For Res 34:465–480

    Article  Google Scholar 

  • Roberts J, Hopkins R, Morecroft M (1999) Towards a predictive description of forest canopies from litter properties. Funct Ecol 13:265–272

    Article  Google Scholar 

  • Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47:235–242

    Article  Google Scholar 

  • Samuelson LJ, McLemore III PC, Somers GL (2003) Relationship between foliar δ13C and hydraulic pathway length in Pinus palustris. For Sci 49:790–798

    Google Scholar 

  • Schleser GH (1990) Investigations of the δ13C pattern in leaves of Fagus sylvatica L. J Exp Bot 41:565–572

    Article  CAS  Google Scholar 

  • Schleser GH, Jayasekara R (1985) δ13C variations of leaves in forests as an indication of reassimilated CO2 from the soil. Oecologia 65:536–542

    Article  Google Scholar 

  • Schulze ED, Kelliher FM, Körner C, Lloyd J, Leuning R (1994) Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: a global scaling exercise. Annu Rev Ecol Syst 25:629–660

    Article  Google Scholar 

  • Sellin A, Kupper P (2004) Within-crown variation in leaf conductance of Norway spruce: effects of irradiance, vapour pressure deficit, leaf water status and plant hydraulic constraints. Ann For Sci 61:419–429

    Article  Google Scholar 

  • Sharkey TD, Raschke K (1981) Separation and measurement of direct and indirect effects of light on stomata. Plant Physiol 68:33–40

    Article  PubMed  Google Scholar 

  • Sparks JP, Ehleringer JR (1997) Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects. Oecologia 109:362–367

    Article  Google Scholar 

  • Stewart GR, Turnbull MH, Schmidt S, Erskine PD (1995) 13C natural abundance in plant communities along a rainfall gradient: a biological integrator of water availability. Aust J Plant Physiol 22:51–55

    Article  Google Scholar 

  • Teskey RO, Fites JA, Samuelson LJ, Bongarten BC (1986) Stomatal and nonstomatal limitations to net photosynthesis in Pinus taeda L. under different environmental conditions. Tree Physiol 2:131–142

    PubMed  Google Scholar 

  • Turney CSM, Hunt JE, Burrows C (2002) Deriving a consistent δ13C signature from tree canopy leaf material for palaeoclimatic reconstruction. New Phytol 155:301–311

    Article  Google Scholar 

  • Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84:362–370

    Google Scholar 

  • von Caemmerer S, Evans JR (1991) Determination of the average partial pressure of CO2 in chloroplasts from leaves of several C3 plants. Aust J Plant Physiol 18:287–305

    CAS  Google Scholar 

  • Walcroft AS, Silvester WB, Grace JC, Carson SD, Waring RH (1996) Effects of branch length on carbon isotope discrimination in Pinus radiata. Tree Physiol 281–286

  • Waring RH, Silvester WB (1994) Variation in foliar δ13C values within tree crowns of Pinus radiata. Tree Physiol 14:1203–1213

    PubMed  Google Scholar 

  • Warren CR, McGrath JF, Adams MA (2001) Water availability and carbon isotope discrimination in conifers. Oecologia 127:476–486

    Article  Google Scholar 

  • Warren CR, Ethier GJ, Livingston NJ, Grant NJ, Turpin DH, Harrison DL, Black TA (2003) Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) canopies. Plant Cell Environ 26:1215–1227

    Article  CAS  Google Scholar 

  • Watts WR, Neilson RE, Jarvis PG (1976) Measurements of stomatal conductance and 14CO2 uptake in a forest canopy. J Appl Ecol 13:623–638

    Article  Google Scholar 

  • Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426

    Article  Google Scholar 

  • Wong SC, Cowan IR, Farquhar GD (1985) Leaf conductance in relation to rate of CO2 assimilation I. Influence of nitrogen nutrition, phosphorus nutrition, photon flux density, and ambient partial pressure of CO2 during ontogeny. Plant Physiol 78:821–825

    PubMed  Google Scholar 

  • Wright GC, Hubick KT, Farquhar GD, Rao RCN (1993) Genetic and environmental variation in transpiration efficiency and its correlation with carbon isotope discrimination and specific leaf area in peanut. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant–water relations. Academic New York

    Google Scholar 

  • Zhang JW, Marshall JD (1995) Variation in carbon isotope discrimination and photosynthetic gas exchange among populations of Pseudotsuga menziesii and Pinus ponderosa in different environments. Funct Ecol 9:402–412

    Article  Google Scholar 

  • Zimmerman JK, Ehleringer JR (1990) Carbon isotope ratios are correlated with irradiance levels in the Panamanian orchid Catasetum viridiflavum. Oecologia 83:247–249

    Article  Google Scholar 

Download references

Acknowledgements

We thank field hands Ben Harlow, Frederique Weber, and Guillaume Ryckelynck, and trusty field and laboratory helper Benjamin Jerabek Miller, and the US Forest Service for permission to work and use the facilities at the Priest River Experimental Forest. Bob Stickrod was largely responsible for accurate stable isotope composition determinations. This project was made possible by a grant from the McIntire-Stennis program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. A. Duursma.

Additional information

Communicated by K. Winter

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duursma, R.A., Marshall, J.D. Vertical canopy gradients in δ13C correspond with leaf nitrogen content in a mixed-species conifer forest. Trees 20, 496–506 (2006). https://doi.org/10.1007/s00468-006-0065-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-006-0065-3

Keywords

Navigation